Anthracnose is a devastating disease caused by Colletotrichum that significantly affects the yield and economic value of the tea plant (Camellia sinensis). However, few studies have addressed the genetic mechanism of anthracnose resistance (AR). This study investigated the QTL associated with AR in a ‘Longjing 43’בBaijiguan’ (LJ43×BJG) population. The field surveys conducted in this study led to the identification of several QTLs for AR on the linkage map. One major QTL (qAR-12.4) accounted for 12% of the phenotypic variance explained over two years. The BSA-seq results also revealed two genomic regions, qARChr1 on chromosome 1 and qARChr13 on chromosome 13, which showed strong correlations with AR. Time-course RNA-seq was performed on LJ43 and BJG inoculated with anthracnose at 0, 24, and 48 hours to screen for candidate genes. The results showed the gradual post-inoculation expression of a nuclear-localized ERF transcription factor (CsERF105) within the qARChr1 locus in BJG but not in LJ43. The AR of BJG was significantly reduced after feeding with CsERF105-specific antisense oligonucleotides, suggesting that CsERF105 may be a positive regulator. The findings of this study add to our general knowledge of the genetic factors involved in the tea plant's AR and potential breeding targets.